Adaptations of the Reed Frog Hyperolius Yiridibayus (Amphibia: Anura: Hyperoliidae) to Its Arid Environment
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J Comp Physiol B (1992) 162:314-326 Joumalof " Biochemical, Compa rat lYe :~:~:';'n Physiology B =Iogy © Springer-Verlag 1992 Adaptations of the reed frog Hyperolius yiridiBayus (Amphibia: Anura: Hyperoliidae) to its arid environment VI. The iridophores in the skin as radiation reflectors F. Kobelt and K.E. Linsenmair* Zoologisches Institut HI, Biozentrum, Am Hubland, W-8700 Wiirzburg, FRG Accepted November 26, 1991 Summary. Hyperolius viridiflavus possesses one complete Introduction layer ofiridophores in the stratum spongiosum of its skin at about 8 days after metamorphosis. The high reflec Members of the "super" species Hyperolius viridiflavus tance of this thin layer is almost certainly the result of (Schi0tz 1971) inhabit seasonally very hot and dry Afri multilayer interference reflection. In order to reflect a can savannas. During dry seasons, these small reed frogs mean of about 35% of the incident radiation across a aestivate unhidden mostly on dry plants. Some aspects spectrum of 300-2900 nm only 30 layers of well-arranged of their water and energy economy and of nitrogen me crystals are required, resulting in a layer 10.5 ~m thick. tabolism have been reported in Geise and Linsenmair These theoretical values are in good agreement with (1986, 1988), Schmuck and Linsenmair (1988) and the actual mean diameter of single iridophores Schmuck et al. (1988). (15.0 ± 3.0 ~m), the number of stacked platelets (40-100) As indicated by the "climate space" parameters (Gates and the measured reflectance of one complete layer of 1980), in dry seasons a skin reflectance higher than 0.7 these cells (32.2 ± 2.3 %). Iridescence colours typical of is vital during the hottest hours around noon; frogs are multilayer interference reflectors were seen after severe exposed to a heavy solar radiation load and air tem dehydration. The skin colour turned from white (0-10% peratures between 38°C and 43 °C (Kobelt and Linsen weight loss) through a copper-like iridescence (10-25% mair 1986). During acclimatization to dry season con weight loss) to green iridescence (25--42%). In dry season ditions a very conspicuous change in the wet-adapted, state, H. viridiflavus needs a much higher reflectance to yellow-brownish colour pattern of juvenile frogs can be cope with the problems of high solar radiation load seen. Skin colour is brownish-white or grey at air tem during long periods with severe dehydration stress. Dry peratures below 35 cc and becomes much paler at air adapted skin contains about 4-6 layers of iridophores. temperatures over 35-37 cc. As acclimatization pro The measured reflectance (up to 60% across the solar gresses this colour approaches brilliant white. These spectrum) of this thick layer (over 60 /-lm) is not in keep changes are accompanied by a thickening of the layer of ing with the results obtained by applying the multilayer light-reflecting iridophores (Bagnara 1976) in most parts interference theory. Light, scattered independently of of the skin from 15 /-lm up to 80 /-lm (Ko belt and Linsen wavelength from disordered crystals, superimposes on mair 1986) and a corresponding increase in the amount the multilayer-induced spectral reflectance. The initial of skin-deposited purines (Schmuck et al. 1988). parallel shift of the multi layer curves with increasing Even as long as a century ago it was assumed that light thickness and the almost constant ("white") reflectance interference was involved in the reflectance of the irido of layers exceeding 60 /-lm clearly point to a changing phores ["Interferenzzellen": Biedermann (1892); van physical basis with increasing layer thickness. Rynberk (1906)]. Denton (1970), in work on the irides cence colours of fish scales, and Land (1966, 1972) in Key words: Arid environment - Aestivation - Irido studies on the eyes of the scallop Pecten maximus, came phores - Skin reflectance - Frog, Hyperolius viridiflavus to the conclusion that iridophores in general might be taeniatus multilayer interference reflectors [see also Rohrlich and Porter (1972), Menter et al. (1979) and Frost and Robin son (1984)]. Huxley (1966) developed a method to cal culate the reflectance of these biological structures. Some morphological aspects of dermal anuran iridophores re * To whom offprint requests should be sent semble the structure of Huxley's reflectors and hence F. Kobelt and K.E. Linsenmair: Adaptations of H. viridiflavus to its arid environment 315 suggest that the reflectance of the anuran skin might be The multilayer interference theory explained by this theory. Many platelets in the iridophores are arranged in The multilayer interference theory for biological systems stacks of 3-20 crystals. In recently metamorphosed wet has been developed by Huxley (1966) and Land (1966). adapted H. viridiflavus these stacks are distributed in an A detailed description of this theory is given in Appen irregular mode. In dry-adapted H. viridiflavus, however, dix B. The reflectance (R) of a multilayer interference a significant alignment is evident, many stacks being structure is given by Eqs. 9a and 9b in Appendix B. From arranged more or less parallel to the surface (Kobelt and this theory the spectral distribution of the reflected light Linsenmair 1986). However, the reflectance of multi layer can be calculated. Comparing them with the measured structures is wavelength selective, and if iridophores are spectral distribution of the light reflected from the skin pure multilayer interference reflectors their reflected light may provide clues to whether the reflecting layer has the should be coloured and not white. physical properties of a multilayer interference structure. Some investigators described three groups of irido phores in fishes (Ballowitz 1912; Connolly 1925; Becher 1929; Foster 1933, 1937; Odiorne 1933; Shanes and Nigrelli 1941; Fries 1942, 1958). One group of cells, Materials and methods leucophores, is situated in the dermis above the bony scale and reflects white light due to scattering of poorly Specimen treatment. Frogs were kept in terraria at 28/24 QC, ordered platelets. Two other groups, iridophores, one in 70/100% relative humidity (day/night) and a light regime of the dermis beneath the bony scale and another one still IlL: 13D to simulate "wet season conditions" (spraying of water and feeding daily) and "transitional conditions" (spraying and deeper and above the muscles, are iridescent due to paral feeding three times a week). "Dry season conditons" were simulated lel-ordered platelets (Denton 1970). These findings sug in an incubator at 30/20 QC, 30/70% relative humidity and IlL: 13D gest that two possible physical mechanisms are involved without feeding. Detailed descriptions of specimen treatment of in the high reflectance of light via iridophores: light H. v. taeniatus for inducing wet and dry season physiological states scattering and multilayer interference. in the laboratory have been presented elsewhere (Geise and Linsen Both physical mechanisms of reflectance provide ad mair 1988; Schmuck and Linsenmair 1988; Schmuck et aI. 1988). vantages and disadvantages: (1) Multilayer interference White reflectance measurements. For these measurements freshly structures can be manufactured very fast and at low transformed froglets were maintained under wet season conditions energy and material costs. Layers of not more than for 2 days and divided into two experimental groups. The amount 10 ~m are highly efficient light reflectors in a given spec of guanine in the skin of these froglets is less variable than in the tral range but are not very efficient across the whole solar juvenile frogs of group 3 which may have access to conditions spectrum. (2) Structures that scatter light independent of inducing dry season acclimatization. wavelength are much more effective reflectors across the Group 1: 14 froglets were kept wet-acclimatized by hydrating them every 24 h for 60 min with 500 III double-distilled water. whole solar spectrum but need much more energy and Group 2: 20 froglets were dry-acclimatized. 500 III of double material. This investigation was performed to decide distilled water was supplied for 15 min only when water losses which physical model best explains the high skin reflec exceeded 30-35% of body weight. All froglets needed a first water tance in fully dry-adapted H. viridiflavus. supply between day 10 and 12. A second supply had to be given with great individual differences mostly between day 30 and day 50 (90% of the froglets). Only about 10% received a second supply before day 30. The Kubelka-M unk-Theory Spectral reflectance measurements. For these measurements wet acclimatized juvenile H. v. taeniatus were used (age 2-4 months after Scattering of white light can be calculated according to metamorphosis). These frogs possess 1-2 complete reflecting layers the Kubelka-Munk-Theory. A summary of theories deal of dermal iridophores. Thus, errors due to iridophore-independent absorption of light deep in the body of the animal, resulting from ing with the optical characteristics of powder layers, in gaps in the reflecting layer which may be present in freshly trans which the layer is considered a continuum, has been formed froglets, are negligible. given by Kortiim (1966). (A detailed description of the Group 3: 16 juvenile frogs were maintained under transition state model and definitions of symbols are given in Appen conditions for 2 weeks and kept under dry season conditions after dix A). When S is estimated from animal data and Ro is wards. Measurement started at the beginning of the dry season measured, the thickness d of a scattering layer in the skin treatment. can be calculated from: Group 4: Ten juvenile frogs were acclimatized and kept for 2-3 months under dry season conditions before measurement. During 1 ) l-R'R this period they developed 4--6 iridophore layers, thereby matching S . d· -- R = In 0 w (4) ( Rw w Ro animals which had been collected in the field after spending a dry 1-- season of comparable duration.